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Utilidad de la punción aspirativa transbronquial guiada
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El salbutamol mejora la contractilidad diafragmática
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Análisis de supervivencia de la cirugía de resección
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Original Article
Survival Analysis of Resection of Lung Metastases From Colorectal Cancer
Roberto Mongil Poce, * Carlos Pagés Navarrete, José Antonio Ruiz Navarrete, a Javier Roca Fernández,
Ricardo Arrabal Sánchez, Agustín Benítez Doménech, Antonio Fernández de Rota Avecilla,
and José Luis Fernández Bermúdez
Servicio de Cirugía Torácica, Hospital Regional Universitario Carlos Haya, Málaga, Spain
ARTICLE INFO
ABSTRACT
Article history:
Received April 24, 2008
Accepted November 27, 2008
Available online April 22, 2009
Introduction: The publication of the International Registry of Lung Metastases (IRLM) in 1997 was a turning
point in favor of surgical resection of lung metastases. Prognostic groups were defined according to
resectability, number of metastases, and disease-free interval. The objective of this study was to determine
survival in patients who underwent resection of lung metastases from colorectal carcinoma and to evaluate
how applicable the prognostic factors established by the IRLM are in this specific patient group.
Patients and Methods: Patients with lung metastases from colorectal carcinoma who underwent resection
between January 1, 2000, and November 30, 2006, were retrospectively analyzed. Survival was calculated
using the Kaplan-Meier method, with log-rank comparisons between groups.
Results: Survivals at 1, 3, 5, and 6 years was 92%, 75%, 54%, and 43%, respectively. The main finding was that
3-year survival was better in patients who underwent atypical resection of the metastasis (75%) than those
who required lobectomy (55%). There were no significant differences in survival in terms of number of
lung metastases resected or disease-free interval.
Conclusions: Survival in patients requiring lobectomy for resection of lung metastases from colorectal
carcinoma was worse than in those who underwent atypical resection. The number of metastases and
disease-free interval may be questionable prognostic factors in the case of lung metastases from colorectal
carcinoma.
© 2008 SEPAR. Published by Elsevier España, S.L. All rights reserved.
Keywords:
Lung metastasis
Colorectal carcinoma
Surgery
Analisis de supervivencia de la cirugía de resección de metastasis pulmonares
de cáncer colorrectal
RESUMEN
Palabras clave:
Metástasis pulmonar
Carcinoma colorrectal
Tratamiento quirúrgico
Introducción: La publicación del Registro Internacional de Metástasis Pulmonares (IRLM, de International
Registry of Lung Metastases) en 1997 supuso un punto de inflexión a favor de la cirugía de resección de
metástasis pulmonares (MP). Se establecieron grupos pronósticos en función de la resecabilidad, el número
de MP y el intervalo libre de enfermedad (ILE). El objetivo de este trabajo ha sido determinar la supervivencia de los pacientes intervenidos con resección de MP de carcinoma colorrectal y evaluar la aplicabilidad de
los factores pronósticos establecidos por el IRLM a este grupo concreto de pacientes.
Pacientes y métodos: Se ha realizado un trabajo retrospectivo recogiendo los casos de MP de carcinoma colorrectal intervenidos entre el 1 de enero de 2000 y el 30 de noviembre de 2006. Para calcular la supervivencia se empleó el método de Kaplan-Meier con el test de rangos logarítmicos.
Resultados: La supervivencia a 1; 3; 5, y 6 años fue del 92, el 75, el 54 y el 43%, respectivamente. Como principal hallazgo, se observó que los pacientes a quienes se realizó resección atípica de las metástasis tuvieron
* Corresponding author:
E-mail address: [email protected] (R. Mongil Poce).
0300-2896/$ - see front matter © 2008 SEPAR. Published by Elsevier España, S.L. All rights reserved.
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236
R. Mongil Poce et al / Arch Bronconeumol. 2009;45(5):235-239
mayor supervivencia que aquellos que necesitaron lobectomía: un 75% de supervivencia a los 3 años frente
al 55%, respectivamente. No se encontraron diferencias significativas de supervivencia en cuanto al número de MP resecadas ni en cuanto al ILE.
Conclusiones: Los pacientes que requieren lobectomía para la resección de MP de carcinoma colorrectal
presentan peor supervivencia que aquellos a los que se realiza resección atípica. El número de metástasis y
el ILE pueden ser factores pronósticos cuestionables en el caso de MP de carcinoma colorrectal.
© 2008 SEPAR. Publicado por Elsevier España, S.L. Todos los derechos reservados.
Introduction
Patients and Methods
The dissemination of neoplastic cells, with the subsequent
appearance of metastases, is the strongest negative prognostic factor
in patients with cancer. Despite the progress made in the prevention
of metastases and multimodal treatment, metastatic disease is still
the main cause of death in these patients.1
Given that the lungs act as the first filter for malignant cells from
a large majority of malignant tumors, lung involvement should not
always be considered a reflection of a systemic neoplastic state. This
idea has led several authors to consider surgical removal of
metastases as part of the therapeutic algorithm for cancer patients.2
The publication, in 1997, of the results of the International Registry
of Lung Metastases (IRLM), with a total of 5206 patients who
underwent surgery at 18 sites in Europe, the United States, and
Canada,3 made a substantial contribution to the consideration of
lung metastasectomy as an effective procedure in terms of survival.
Analysis of the data led to the development of a prognostic model
comprising 4 groups defined according to the number of lung
metastases, their resectability, and the disease-free interval (DFI)
from treatment of the primary tumor until the appearance of the
lung metastasis (Table).
Colorectal cancer is one of the most common malignant diseases
in industrialized countries.4,5 It has been estimated that more than
148 000 new cases were diagnosed in 2006 in the USA alone and that
more than 55 000 patients died as a result of the disease in that
year.6 Approximately 10% of patients with colorectal cancer suffer
lung metastases, although the lung is the exclusive site of metastasis
in only 2% to 4% of all patients.7
Although chemotherapy as treatment of metastatic colorectal
cancer has advanced a great deal in the last decade, achieving a
median survival of 20 to 22 months, 5-year survival of patients not
eligible for rescue surgery is still less than 5%.8 No prospective,
randomized trials have yet been undertaken to compare the outcome
of surgical removal of lung metastases from colorectal cancer with
the outcome of other nonsurgical treatments. Resection of lung
metastases from colorectal carcinoma therefore remains the only
potentially curative treatment.9
The objective of this study was to analyze survival and prognosis
in patients who underwent resection of lung metastases from
colorectal carcinoma with curative intent. In addition, the study
aimed to confirm the validity of the prognostic factors proposed by
the IRLM when applied to a series of patients with lung metastases
exclusively from colorectal carcinoma.
We performed a retrospective analysis of all resection procedures
for lung metastases from colorectal carcinoma with curative intent
performed consecutively in the Thoracic Surgery Department of the
Hospital Regional Universitario Carlos Haya, Málaga, Spain, between
January 2000 and November 2006. The medical histories of the
patients who underwent surgery during the study period were
reviewed. Surgical procedures performed exclusively for diagnostic
purposes were excluded.
Lung metastases from colorectal carcinoma were resected
provided the following conditions were met: unilateral or bilateral
resectable pulmonary nodules detected by chest computed
tomography (CT); absence of local recurrence of the primary tumor;
absence of extrapulmonary metastases (except for resected or
resectable liver metastases); and, finally, compliance with the criteria
for operability applicable to any type of intervention involving lung
resection. In most cases, a helical system was used for the chest CT,
with 10 mm slices.
The standard procedure for this type of surgery was extensive
palpation of the entire lung parenchyma by the surgeons and their
assistant or assistants, with resection of all palpable nodules, while
respecting as much healthy parenchyma as possible. The nodules
were subsequently submitted for definitive clinicopathologic
diagnosis. Systematic lymph node dissection was not employed, and
lymph nodes were only resected during the intervention when there
was visible evidence of disease.
The variables studied were age and sex of the patients, number of
resected metastases per procedure, DFI (time from treatment of the
primary tumor until detection of the metastasis), surgical approach,
type of lung resection, agreement between the number of metastases
detected in the chest CT and those confirmed by the definitive
clinicopathology study, postoperative complications, and survival of
patients operated between January 1, 2000, and November 30, 2006.
The survival of the patients was ascertained by a telephone call or
directly by a visit to the outpatient clinic.
Statistical Analysis
For the statistical analysis, descriptive statistics, contingency
tables, and the χ2 test were used. Kaplan-Meier survival curves were
compared with the log rank test. Statistical analysis was performed
using version 12.0 of the Statistical Package for Social Sciences (SPSS,
Chicago, Illinois, USA) for Windows.
Results
Table
Prognostic Groups and Factors in Lung Metastasis Resection According to the
International Registry for Lung Metastases (1997)
Group 1
Group 2
Group 3
Group 4
Resectable, with no risk factors (DFI of 36 months and solitary
metastasis)
Resectable, with 1 risk factor (DFI<36 months or multiple metastases)
Resectable, with 2 risk factors (DFI<2 months and multiple metastases)
Unresectable
Abbreviation: DFI, disease-free interval.
Between January 1, 2000, and November 30, 2006, 126 lung
metastases, were resected with curative intent from 106 patients
(Figure 1). Of these procedures, 54 were resections of lung metastases
from colorectal cancer in 45 patients.
The age range of patients undergoing surgery was 38 to 81 years,
with a mean age of 62.9 years. Twenty-five of these patients were
men (31 procedures) and 20 were women (23 procedures). A single
metastasis was resected in 63.8% of the procedures, whereas 2 were
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R. Mongil Poce et al / Arch Bronconeumol. 2009;45(5):235-239
resected in 23.4%, 3 in 8.5%, and 4 in 4.3%. Only 6 patients (13.3%) had
metastases in both lungs at the time of diagnosis. In 25% of the
procedures, palpation during surgery detected a greater number of
metastases than previously detected in chest CT. The DFI was
between 0 and 11 months in 21.6% of the patients, between 12 and
35 months in 32.4%, and greater than 36 months in 45.9%.
A posterolateral thoracotomy was performed in 46 patients
(85.18%), lateral thoracotomy in 2 patients, and simultaneous
bilateral thoracotomy in a single patient with metastases in both
lungs. In 4 procedures (7.7%), video-assisted thoracoscopy was used
to rule out pleural invasion by the metastases before thoracotomy.
Sternotomy was only done in 1 patient.
Of the resections, 35 were atypical (64.81%), 5 were segmentectomies
(9.25%), 8 were simple lobectomies (14.81%), 1 was a bilobectomy,
1 was a sleeve lobectomy, 2 were lobectomies plus atypical resection,
and 2 were atypical resections with removal of a part of the chest wall.
No postoperative complications were reported in 90.2% of the
procedures. An air leak lasting more than 7 days, postoperative ileus,
postoperative respiratory failure, and chylothorax which resolved
with conservative management were experienced by 1 patient each.
Only 1 postoperative death occurred (that is, within 30 days of the
surgical procedure) due to pulmonary thromboembolism.
The mean postoperative stay was 8.63 days.
Survival at 1, 3, 5, and 6 years after the operation was 92%, 75%,
54%, and 43%, respectively, with a mean survival of 73.22 months
(Figure 2) and a median survival of 66.6 months. There were no
60
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50
40
34
30
26
24
18
20
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12
10
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Figure 1. Change in the number of interventions for lung metastases in our department
from 1991 to 2006.
1.0
Cumulative Survival
0.9
0.8
0.7
0.6
0.5
0.4
0
12
24
36
48
60
Time, m
72
84
96
Figure 2. Survival in patients who underwent resection of lung metastases from
colorectal carcinoma.
237
significant differences in survival according to sex, surgical approach,
number of metastases, or DFI. In contrast, significant differences
were reported according to the type of resection: 3-year survival in
cases of atypical resection was 75%, with a mean survival of 94.41
months, compared to a 3-year survival of 55% and mean survival of
31.9 months in cases of lobectomy.
Discussion
Since the publication of the results of the IRLM,3 resection of lung
metastases with therapeutic intent has become a frequent indication
in thoracic surgery departments.
The study by Pastorino et al3 marks a watershed in surgical
resection of lung metastases. As it was a multicenter study, the
investigators were able to collect data from 5206 patients, making it
the largest study to date on the subject. Its most important
contribution was to establish prognostic groups defined according to
the presence of certain risk factors: resectability, number of
metastases, and DFI. The main drawback of the study was that the
influence of prognostic factors specific to each type of primary tumor
was not analyzed.10 Although the results have been validated in
other case series involving resection of lung metastases from
different origins,11 their applicability to a case series of patients with
lung metastases exclusively from colorectal cancer has never been
assessed.10
Two of the most important aspects to take into account with this
type of surgery are the approach and the type of resection performed.
One of the determining factors in the choice of approach is the
disagreement between prior radiologic findings and definitive
clinicopathologic ones. In our series, 25% more lung metastases were
detected in the histopathologic study than in conventional chest CT
performed before surgery. Even in recent studies with helical CT
with 5-mm slices, the sensitivity for detecting lesions of less than
6 mm in diameter was still limited.12-14
Some authors are in favor of using video-assisted thoracoscopy
when resecting lung metastases with curative intent,15,16 arguing
that it is less aggressive than other approaches, with a subsequent
decrease in postoperative pain, complications, and duration of
hospital stay. However, one of the strongest arguments against the
use of video-assisted thoracoscopy for resection of lung metastases
is provided by McCormack et al17 in their much cited prospective
study conducted at the Memorial Sloan-Kettering Cancer Center.
That study, which aimed to compare video-assisted thoracoscopy
with thoracotomy, had planned to include 50 patients but had to be
terminated prematurely after only 18 patients had been enrolled
because a statistically significant benefit was detected in terms of
the number of metastases found with thoracotomy.
Currently, any thoracic approach for resection of lung metastases
has to meet 3 essential requirements2,18: it has be as unaggressive as
possible, allow manual palpation, and allow resection of all palpable
metastases.
As mentioned above, video-assisted thoracoscopy has a minimal
morbidity and offers excellent visualization of subpleural nodules
but its capacity for locating small and intraparenchymatous nodules
has been found wanting.19,20 However, despite the disagreement
between radiologic and clinicopathologic findings, recently published
studies in series of patients with resected lung metastases using
video-assisted thoracoscopy have reported similar results to those
achieved with thoracotomy in terms of long-term survival.21,22
Indeed, Pfannschmidt et al,23 in their recent review, concluded that
although thoracotomy continues to be the most widely used
approach for resection of lung metastases from colorectal carcinoma,
video-assisted thoracoscopy may play an important role in the
resection of peripheral lung metastases.
In the series presented here, the main approach used was
posterolateral thoracotomy. This approach allows the whole of the
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238
R. Mongil Poce et al / Arch Bronconeumol. 2009;45(5):235-239
lung parenchyma to be palpated and resection of all palpable nodules.
In cases of bilateral metastases, one side of the thorax is treated and
the patient allowed to recover before operating on the other side
(after approximately 3 weeks). Simultaneous bilateral thoracotomy
is only used in young patients with good functional capacity as this
approach may substantially affect respiration in the immediate
postoperative period.
The choice of type of resection for removal of the lung metastases
is based on 2 essential considerations—resection of all nodules with
a healthy lung tissue margin while being as conservative as possible
in terms of respecting the parenchyma.2 Thus, metastasectomy or
atypical resection of the metastatic nodule, preferably using surgical
staplers, is the technique of choice as it is safe, associated with
limited morbidity and mortality, and is just as effective as routine
lung resections.24,25 Pneumonectomy and/or removal of adjacent
tissue is usually not indicated, except in certain exceptional
cases.2,24
In the series presented here, the most relevant finding was that
patients who underwent an atypical resection of metastases
survived significantly longer than those who underwent major
anatomical resections (lobectomies): 3-year survival in cases of
atypical resection was 75%, with a mean survival of 94.41 months,
compared to 3-year survival of 55% and mean survival of
31.9 months in cases of lobectomy. This difference may be because
patients requiring lobectomies had more advanced disease given
the larger size of the metastases, although this variable was not
statistically significant in our series. A greater volume of visibly
diseased tissue indicates a greater likelihood that other undetectable
metastases are present.10
This finding, in line with that published by Vogelsang et al,26
supports the traditional approach of attempting to resect all nodules
while endeavoring to respect as much healthy parenchyma as
possible, firstly, because further metastasectomies may have to be
performed in the event of relapse and, secondly, because of the
worse survival in cases of larger resections.
In contrast to the findings of the IRLM, in our study, we did not
see any significant differences in survival according to the number of
metastases or DFI, in agreement with the study published recently
by Muñoz-Llarena et al.10 In that study, not even dividing the patients
into the prognostic groups of the IRLM, which include both number
of metastases and DFI, yielded a different course among patients,
prompting the authors to claim that those variables are of
questionable use as prognostic factors in lung metastases from
colorectal cancer. Those conclusions, although derived from
retrospective studies, are in line with other recently published
studies that cast doubt on what have been considered the underlying
principles in the treatment of lung metastases from colorectal cancer
until now. Pfannschmidt et al,23 in their recent review, did not find
the DFI to be a significant long-term prognostic factor, although they
did think it followed that patients with a solitary lung metastasis
benefit more from resection than those with multiple metastases.
For their part, Tanaka et al27 concluded that the optimum moment,
in terms of survival, for resecting lung metastases from colorectal
carcinoma is at least 3 months after radiologic diagnosis. We
underline that these findings need to be confirmed in randomized,
prospective studies in the future.
The percentage of postoperative complications reported in this
series is similar to that published by the IRLM: 4.9% of serious
complications, with a perioperative mortality of 1.7%.
With respect to overall survival, the results obtained in this series
(54% survival at 5 years, with a mean survival of 73.22 months) lie
within the ranges published to date: 38.3% to 63.7% with a median of
52.5%.23 Many of the patients received adjuvant chemotherapy after
resection of the metastases and, although this variable was not
analyzed, it may contribute to the more than acceptable survival in
this group of patients. This aspect has already been proposed recently
by more than one author,10,23 and should perhaps be investigated in
future studies.
In conclusion, resection of lung metastases from colorectal
carcinoma is an effective therapeutic option for improving survival
and one that is increasingly requested. Morbidity and mortality are
relatively low. This approach remains the one that allows sufficient
and extensive palpation of the entire lung parenchyma to detect
metastases that do not show up with conventional radiologic
techniques. Video-assisted thoracoscopy would seem to be indicated
in some patients with peripheral metastases.21-23 The type of resection
should be one that allows the metastasis to be removed while
respecting as much healthy lung parenchyma as possible, that is,
mayor lung resections, such as lobectomies and pneumonectomies,
should be avoided as far as possible. In the series presented, mediumterm survival in patients undergoing atypical resections was better
than in those undergoing other procedures. The number of lung
metastases and the DFI are questionable as prognostic factors in
patients with lung metastases from colorectal cancer. Last but not
least, evidence in favor of resection of lung metastases has so far
been based on retrospective analyses of case series.23 Therefore, it is
necessary to conduct prospective randomized studies comparing
outcomes (in terms of survival and quality of life) after resection of
lung metastases from colorectal carcinoma with those obtained after
other nonsurgical therapeutic approaches in order to offer the best
possible care to this group of patients.28
Acknowledgments
The members of the Thoracic Surgery Department of the HRU
Carlos Haya de Málaga wish to express our gratitude to Dr José Luis
Fernández Bermúdez and Dr Antonio Fernández de Rota Avecilla for
their life work dedicated to medicine and their role as pioneers of
thoracic surgery in Málaga. We hope this study serves as recognition
of that work.
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